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Co-Evolution of Epibiotic Bacteria Associated with the Novel

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Co-Evolution of Epibiotic Bacteria Associated with the Novel Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution 1*Edgcomb, V.P., 2Breglia, S.A., 2Yubuki, N., 3Beaudoin, D., 4Patterson, D.J., 2Leander, B.S. and 1Bernhard, J.M. 1Woods Hole Oceanographic Institution, Geology and Geophysics Department, Woods Hole, MA 02543, USA 2Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, Departments of Botany and Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada 3Woods Hole Oceanographic Institution, Biology Department, Woods Hole, MA 02543, USA 4Marine Biological Laboratory, Biodiversity Informatics, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA. Running title: Identity of epibionts on symbiontid euglenozoans Keywords: Symbiontida, epibionts, epsilon-proteobacteria, Calkinsia, Bihospites, co-evolution, sulfide Subject categories: 1) Microbe-microbe and microbe-host interactions 2) Evolutionary genetics *Corresponding author Abstract A distinct subgroup of euglenozoans, referred to as the “Symbiontida,” has been described from oxygen-depleted and sulfidic marine environments. By definition, all members of this group carry epibionts that are intimately associated with underlying mitochondrion-derived organelles beneath the surface of the hosts. We have used molecular phylogenetic and ultrastructural evidence to identify the rod-shaped epibionts of two members of this group, Calkinsia aureus and Bihospites bacati, hand-picked from sediments from two separate oxygen-depleted, sulfidic environments. We identify their epibionts as closely related sulfur or sulfide oxidizing members of the Epsilon proteobacteria. The Epsilon proteobacteria generally play a significant role in deep-sea habitats as primary colonizers, primary producers, and/or in symbiotic associations. The epibionts likely fulfill a role in detoxifying the immediate surrounding environment for these two different hosts. The nearly identical rod-shaped epibionts on these two symbiontid hosts provides evidence for a co-evolutionary history between these two sets of partners. This hypothesis is supported by congruent tree topologies inferred from 18S and 16S rDNA from the hosts and bacterial epibionts, respectively. The eukaryotic hosts likely serve as a motile substrate that delivers the epibionts to the ideal locations with respect to the oxic/anoxic interface whereby their growth rates can be maximized, perhaps also allowing the host to cultivate a food source. Because symbiontid isolates and additional SSU rDNA gene sequences from this clade have now been recovered from many locations worldwide, the Symbiontida are likely more widespread and diverse than presently known. 2 Introduction Examples of symbiotic relationships between prokaryotes and eukaryotes in deep sea oxygen depleted marine environments have been well documented for some groups, starting with the discovery of associations between metazoa and bacteria at hydrothermal vents (Cavanaugh et al., 1981), cold seeps (Barry et al., 1996) and the edges of silled basins (e.g. (Distel and Felbeck, 1988). Chemosynthetic autotrophy supports many of these associations and involves the oxidation of hydrogen sulfide or methane by endosymbiotic bacteria within the animal hosts. Similar associations have also been observed between prokaryotes and marine protists. These include a wide range of metabolic relationships observed in shallow marine, primarily reducing environments, including endosymbiotic methanogens in ciliates to epibiotic hydrogen-sulfide oxidizers on euglenids (Epstein et al., 1998; Fenchel et al., 1995; Ott, 1996). The first observations of episymbiotic relationships between protists and prokaryotes in the deep sea were documented in cold seeps of Monterey Bay, CA (Buck and Barry, 1998; Buck et al., 2000) and in the oxygen-depleted Santa Barbara Basin, CA (Bernhard et al., 2000; Bernhard et al., 2010). Both sites were at water depths greater than 500 m, and had high concentrations of mat-forming chemoautotrophic bacteria. In Santa Barbara Basin bottom water, oxygen concentration rarely exceeds 5 µmol L-1 (~0.1 ml L-1) (Kuwabara et al., 1999) and sulfide concentration can exceed 50 µM between 0.5-1.0 cm depth (Bernhard, 2003; Bernhard et al., 2003). In this environment, euglenozoan flagellates (including Calkinsia aureus) were numerically the most abundant group and most eukaryotic taxa harboured bacterial epibionts and/or endosymbionts (Bernhard et al., 2000). The Euglenozoa comprises a large group of flagellates with diverse nutritional modes, and consists of four distinct subgroups: euglenids, kinetoplastids, diplonemids, and symbiontids. 3 Calkinsia aureus, Bihospites bacati, and Postgaardi mariagerensis have been isolated from oxygen-depleted marine environments; each is covered with rod-shaped epibiotic bacteria (Bernhard et al., 2000; Breglia et al., 2010; Simpson et al., 1997a; Yubuki et al., 2009). All three of these species have been characterized at the ultrastructural level, and C. aureus and B. bacati have also been characterized at the molecular phylogenetic level using small subunit (SSU) rDNA sequences (Breglia et al., 2010; Simpson et al., 1997a; Yubuki et al., 2009). The data from C. aureus and B. bacati demonstrated a distinct subgroup of euglenozoans from oxygen- depleted environments (including seven environmental DNA sequences from Northern Europe and South America) referred to as the “Symbiontida.” Symbiontid isolates and additional SSU rDNA sequence representatives of the clade have now been recovered from seafloor sediments of Santa Barbara Basin, CA, coastal sediments of British Columbia, Canada, Northern Germany, and anoxic and sulfidic waters in Venezuela, Denmark and Norway (Breglia et al., 2010; Yubuki et al., 2009). The rod-shaped epibionts of C. aureus are 3-5 µm long and 0.350 µm wide and form a tightly-packed coat over the entire surface of the host cell, with at least 128 bacterial cells observed in a transverse section through C. aureus (Yubuki et al., 2009). Moreover, the distinctively orange color of C. aureus is attributable to a complex extracellular matrix. The prolate-shaped cells of C. aureus are around 48 µm (42.6-71.3µm) long and around 17 µm (14.2- 19.5µm) wide (for a detailed ultrastructure analysis see Yubuki et al. (2009). Unlike most of their euglenozoan relatives (e.g., kinetoplastids and euglenids), C. aureus lacks recognizable mitochondria with cristae, and instead possesses superficially arranged double-membrane bound organelles nearly identical in morphology to the well-described hydrogenosomes found in flagellates from other anoxic environments (Fenchel and Finlay, 1995). Hydrogenosomes 4 function to produce molecular hydrogen, acetate, CO2 and ATP in anoxic environments (Barbera et al., 2007). Bihospites bacati, which was recovered from oxygen-depleted sandy sediments in a shallow tidal flat in South-western British Columbia, Canada, is 40-120 µm long and 15-30 µm wide and the cell surface is covered with two different morphotypes of epibionts: (1) Spherical- shaped bacteria about 0.6µm in diameter with an extrusive apparatus and (2) rod-shaped bacteria 3-5µm long and arranged in bands along the longitudinal axis of the host (Breglia et al., 2010). Longitudinal bands of rod-shaped bacteria were separated by single or double rows of spherical- shaped bacteria. Molecular phylogenetic analyses of small subunit (SSU) rRNA gene sequences demonstrated that to date B. bacati is positioned as the earliest diverging known representative of the Symbiontida, a position consistent with comparative ultrastructure. Several morphological features of B. bacati are transitional between those found in C. aureus and those found in phagotrophic euglenids. Although these ultrastructural data suggest that the Symbiontida is nested within the Euglenida, current molecular phylogenetic data do not shed any light on this hypothesis (Breglia et al., 2010). C. aureus and B. bacati, share the feature of a coupling of rod- shaped epibionts with a superficial layer of hydrogenosome-like, mitochondrion-derived organelles having reduced or absent cristae. This appears to be a unifying characteristic of the Symbiontida, and suggests a mutualistic relationship that has enabled symbiontids to diversify within oxygen-depleted environments. In addition to C. aureus and B. bacati, other euglenozoans from oxygen-depleted environments have been identified with epibiotic bacteria, including Postgaardi mariagerensis (Fenchel et al., 1995; Simpson et al., 1997), Euglena helicoideus (Leander and Farmer, 2000), Dylakosoma pelophilum (Wolowski, 1995), and five unidentified euglenozoans (Bernhard et al., 5 2000; Buck et al., 2000; Buck and Bernhard, 2002). Hypotheses for the biological role(s) of rod shaped epibionts of eukaryotic hosts usually involve commensalism, with the bacteria benefiting from metabolic byproducts secreted by the host (Fenchel et al., 1995; Leander and Keeling, 2004; Simpson et al., 1997). It has also been hypothesized that the epibionts might be chemoautotrophic sulfur- or methane-oxidizers that form a mutualistic relationship with the host, whereby the host provides a substrate for the bacteria and the bacteria detoxify the immediate environment for the host (Bernhard, 2003; Bernhard et al., 2010; Bernhard et al., 2003). Under certain conditions, the epibiotic bacteria may serve as food for the host (Breglia et al., 2010). In order to better understand
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